Sublethal effects of parasitism on ruminants can have cascading consequences for ecosystems.

Parasitic infections are common, but how they shape ecosystem-level processes is understudied. Using a mathematical model and meta-analysis, we explored the potential for helminth parasites to trigger trophic cascades through lethal and sublethal effects imposed on herbivorous ruminant hosts after infection. First, using the model, we linked negative effects of parasitic infection on host survival, fecundity, and feeding rate to host and producer biomass. Our model, parameterized with data from a well-documented producer­caribou­helminth system, reveals that even moderate impacts of parasites on host survival, fecundity, or feeding rate can have cascading effects on ruminant host and producer biomass. Second, using meta-analysis, we investigated the links between helminth infections and traits of free-living ruminant hosts in nature. We found that helminth infections tend to exert negative but sublethal effects on ruminant hosts. Specifically, infection significantly reduces host feeding rates, body mass, and body condition but has weak and highly variable effects on survival and fecundity. Together, these findings suggest that while helminth parasites can trigger trophic cascades through multiple mechanisms, overlooked sublethal effects on nonreproductive traits likely dominate their impacts on ecosystems. In particular, by reducing ruminant herbivory, pervasive helminth infections may contribute to a greener world.

Improve animal health to reduce livestock emissions: quantifying an open goal.

Greenhouse gas (GHG) emissions from livestock production must be urgently tackled to substantially reduce their contribution to global warming. Simply reducing livestock numbers to this end risks impacting negatively on food security, rural livelihoods and climate change adaptation. We argue that significant mitigation of livestock emissions can be delivered immediately by improving animal health and hence production efficiency, but this route is not prioritized because its benefits, although intuitive, are poorly quantified. Rigorous methodology must be developed to estimate emissions from animal disease and hence achievable benefits from improved health through interventions. If, as expected, climate change is to affect the distribution and severity of health conditions, such quantification becomes of even greater importance. We have therefore developed a framework and identified data sources for robust quantification of the relationship between animal health and greenhouse gas emissions, which could be applied to drive and account for positive action. This will not only help mitigate climate change but at the same time promote cost-effective food production and enhanced animal welfare, a rare win-win in the search for a sustainable planetary future.

Natural resistance to worms exacerbates bovine tuberculosis severity independently of worm coinfection.

Pathogen interactions arising during coinfection can exacerbate disease severity, for example when the immune response mounted against one pathogen negatively affects defense of another. It is also possible that host immune responses to a pathogen, shaped by historical evolutionary interactions between host and pathogen, may modify host immune defenses in ways that have repercussions for other pathogens. In this case, negative interactions between two pathogens could emerge even in the absence of concurrent infection. Parasitic worms and tuberculosis (TB) are involved in one of the most geographically extensive of pathogen interactions, and during coinfection worms can exacerbate TB disease outcomes. Here, we show that in a wild mammal natural resistance to worms affects bovine tuberculosis (BTB) severity independently of active worm infection. We found that worm-resistant individuals were more likely to die of BTB than were nonresistant individuals, and their disease progressed more quickly. Anthelmintic treatment moderated, but did not eliminate, the resistance effect, and the effects of resistance and treatment were opposite and additive, with untreated, resistant individuals experiencing the highest mortality. Furthermore, resistance and anthelmintic treatment had nonoverlapping effects on BTB pathology. The effects of resistance manifested in the lungs (the primary site of BTB infection), while the effects of treatment manifested almost entirely in the lymph nodes (the site of disseminated disease), suggesting that resistance and active worm infection affect BTB progression via distinct mechanisms. Our findings reveal that interactions between pathogens can occur as a consequence of processes arising on very different timescales.

Within-host and external environments differentially shape ß-diversity across parasite life stages.

Uncovering drivers of community assembly is a key aspect of learning how biological communities function. Drivers of community similarity can be especially useful in this task as they affect assemblage-level changes that lead to differences in species diversity between habitats. Concepts of ß-diversity originally developed for use in free-living communities have been widely applied to parasite communities to gain insight into how infection risk changes with local conditions by comparing parasite communities across abiotic and biotic gradients. Factors shaping ß-diversity in communities of immature parasites, such as larvae, are largely unknown. This is a key knowledge gap as larvae are frequently the infective life-stage and understanding variation in these larval communities is thus key for disease prevention. Our goal was to uncover links between ß-diversity of parasite communities at different life stages; therefore, we used gastrointestinal nematodes infecting African buffalo in Kruger National Park, South Africa, to investigate within-host and extra-host drivers of adult and larval parasite community similarity. We employed a cross-sectional approach using PERMANOVA that examined each worm community at a single time point to assess independent drivers of ß-diversity in larvae and adults as well as a longitudinal approach with path analysis where adult and larval communities from the same host were compared to better link drivers of ß-diversity between these two life stages. Using the cross-sectional approach, we generally found that intrinsic, within-host traits had significant effects on ß-diversity of adult nematode communities, while extrinsic, extra-host variables had significant effects on ß-diversity of larval nematode communities. However, the longitudinal approach provided evidence that intrinsic, within-host factors affected the larval community indirectly via the adult community. Our results provide key data for the comparison of community-level processes where adult and immature stages inhabit vastly different habitats (i.e. within-host vs. abiotic environment). In the context of parasitism, this helps elucidate host infection risk via larval stages and the drivers that shape persistence of adult parasite assemblages, both of which are useful for predicting and preventing infectious disease.

Season and prey identity mediate the effect of predators on parasites in rodents: a test of the healthy herds hypothesis.

The healthy herds hypothesis (HHH) suggests that predators decrease parasitism in their prey. Repeated tests of this hypothesis across a range of taxa and ecosystems have revealed significant variation in the effect of predators on parasites in prey. Differences in the response to predators (1) between prey taxa, (2) between seasons, and (3) before and after catastrophic disturbance are common in natural systems, but typically ignored in empirical tests of the HHH. We used a predator exclusion experiment to measure the effect of these heterogeneities on the tri-trophic interaction among predators, parasites and prey. We experimentally excluded mammalian predators from the habitats of hispid cotton rats (Sigmodon hispidus) and cotton mice (Peromyscus gossypinus) and measured the effect of exclusion on gastrointestinal parasites in these rodents. Our experiment spanned multiple seasons and before and after a prescribed burn. We found that the exclusion of the same predators had opposite effects on the parasites of small mammal prey species. Additionally, we found that the effect of mammal exclusion on parasitism differed before versus after fire disturbance. Finally, we saw that the effect of predator exclusion was highly dependent on prey capture season. Significant effects of exclusion emerged primarily in the fall and winter months. The presence of so many different effects in one relatively simple system suggests that predator effects on parasites in prey are highly context dependent.

Do predators keep prey healthy or make them sicker? A meta-analysis.

Ecological theory suggests that predators can either keep prey populations healthy by reducing parasite burdens or alternatively, increase parasitism in prey. To quantify the overall magnitude and direction of the effect of predation on parasitism in prey observed in practice, we conducted a meta-analysis of 47 empirical studies. We also examined how study attributes, including parasite type and life cycle, habitat type, study design, and whether predators were able to directly consume prey contributed to variation in the predator-prey-parasite interaction. We found that the overall effect of predation on parasitism differed between parasites and parasitoids and that whether consumptive effects were present, and whether a predator was a non-host spreader of parasites, were the most important traits predicting the parasite response. Our results suggest that the mechanistic basis of predator-prey interactions strongly influences the effects of predators on parasites and that these effects, although context dependent, are predictable.

Bovine tuberculosis disturbs parasite functional trait composition in African buffalo.

Novel parasites can have wide-ranging impacts, not only on host populations, but also on the resident parasite community. Historically, impacts of novel parasites have been assessed by examining pairwise interactions between parasite species. However, parasite communities are complex networks of interacting species. Here we used multivariate taxonomic and trait-based approaches to determine how parasite community composition changed when African buffalo (Syncerus caffer) acquired an emerging disease, bovine tuberculosis (BTB). Both taxonomic and functional parasite richness increased significantly in animals that acquired BTB than in those that did not. Thus, the presence of BTB seems to catalyze extraordinary shifts in community composition. There were no differences in overall parasite taxonomic composition between infected and uninfected individuals, however. The trait-based analysis revealed an increase in direct-transmitted, quickly replicating parasites following BTB infection. This study demonstrates that trait-based approaches provide insight into parasite community dynamics in the context of emerging infections.

Co-infection best predicts respiratory viral infection in a wild host.

The dynamics of directly transmitted pathogens in natural populations are likely to result from the combined effects of host traits, pathogen biology, and interactions among pathogens within a host. Discovering how these factors work in concert to shape variation in pathogen dynamics in natural host-multi-pathogen systems is fundamental to understanding population health. Here, we describe temporal variation in incidence and then elucidate the effect of hosts trait, season and pathogen co-occurrence on host infection risk using one of the most comprehensive studies of co-infection in a wild population: a suite of seven directly transmitted viral and bacterial respiratory infections from a 4-year study of 200 free-ranging African buffalo Syncerus caffer. Incidence of upper respiratory infections was common throughout the study-five out of the seven pathogens appeared to be consistently circulating throughout our study population. One pathogen exhibited clear outbreak dynamics in our final study year and another was rarely detected. Co-infection was also common in this system: The strongest indicator of pathogen occurrence for respiratory viruses was in fact the presence of other viral respiratory infections. Host traits had minimal effects on odds of pathogen occurrence but did modify pathogen-pathogen associations. In contrast, only season predicted bacterial pathogen occurrence. Though a combination of environmental, behavioural, and physiological factors work together to shape disease dynamics, we found pathogen associations best determined infection risk. Our study demonstrates that, in the absence of very fine-scale data, the intricate changes among these factors are best represented by co-infection.

Opposite outcomes of coinfection at individual and population scales.

Coinfecting parasites and pathogens remain a leading challenge for global public health due to their consequences for individual-level infection risk and disease progression. However, a clear understanding of the population-level consequences of coinfection is lacking. Here, we constructed a model that includes three individual-level effects of coinfection: mortality, fecundity, and transmission. We used the model to investigate how these individual-level consequences of coinfection scale up to produce population-level infection patterns. To parameterize this model, we conducted a 4-y cohort study in African buffalo to estimate the individual-level effects of coinfection with two bacterial pathogens, bovine tuberculosis (bTB) and brucellosis, across a range of demographic and environmental contexts. At the individual level, our empirical results identified bTB as a risk factor for acquiring brucellosis, but we found no association between brucellosis and the risk of acquiring bTB. Both infections were associated with reductions in survival and neither infection was associated with reductions in fecundity. The model reproduced coinfection patterns in the data and predicted opposite impacts of coinfection at individual and population scales: Whereas bTB facilitated brucellosis infection at the individual level, our model predicted the presence of brucellosis to have a strong negative impact on bTB at the population level. In modeled populations where brucellosis was present, the endemic prevalence and basic reproduction number ([Formula: see text]) of bTB were lower than in populations without brucellosis. Therefore, these results provide a data-driven example of competition between coinfecting pathogens that occurs when one pathogen facilitates secondary infections at the individual level.

Exposure to Ebola Virus and Risk for Infection with Malaria Parasites, Rural Gabon.

An association between malaria and risk for death among patients with Ebola virus disease has suggested within-host interactions between Plasmodium falciparum parasites and Ebola virus. To determine whether such an interaction might also influence the probability of acquiring either infection, we used a large snapshot surveillance study from rural Gabon to test if past exposure to Ebola virus is associated with current infection with Plasmodium spp. during nonepidemic conditions. We found a strong positive association, on population and individual levels, between seropositivity for antibodies against Ebola virus and the presence of Plasmodium parasites in the blood. According to a multiple regression model accounting for other key variables, antibodies against Ebola virus emerged as the strongest individual-level risk factor for acquiring malaria. Our results suggest that within-host interactions between malaria parasites and Ebola virus may underlie epidemiologic associations.

Risk alleles for tuberculosis infection associate with reduced immune reactivity in a wild mammalian host.

Integrating biological processes across scales remains a central challenge in disease ecology. Genetic variation drives differences in host immune responses, which, along with environmental factors, generates temporal and spatial infection patterns in natural populations that epidemiologists seek to predict and control. However, genetics and immunology are typically studied in model systems, whereas population-level patterns of infection status and susceptibility are uniquely observable in nature. Despite obvious causal connections, organizational scales from genes to host outcomes to population patterns are rarely linked explicitly. Here we identify two loci near genes involved in macrophage (phagocyte) activation and pathogen degradation that additively increase risk of bovine tuberculosis infection by up to ninefold in wild African buffalo. Furthermore, we observe genotype-specific variation in IL-12 production indicative of variation in macrophage activation. Here, we provide measurable differences in infection resistance at multiple scales by characterizing the genetic and inflammatory variation driving patterns of infection in a wild mammal.

Immune stability predicts tuberculosis infection risk in a wild mammal.

Immunity is one of the most variable phenotypic traits in animals; however, some individuals may show less fluctuation in immune traits, resulting in stable patterns of immune variation over time. It is currently unknown whether immune variation has consequences for infectious disease risk. In this study, we identified moderately stable immune traits in wild African buffalo and asked whether the stability of these traits affected bovine tuberculosis (TB) infection risk. We found that adaptive immune traits such as the level of interferon-γ (IFN-γ) released after white blood cell stimulation, the number of circulating lymphocytes and the level of antibodies against bovine adenovirus-3 were moderately repeatable (i.e. stable) over time, whereas parameters related to innate immunity either had low repeatability (circulating eosinophil numbers) or were not repeatable (e.g. neutrophil numbers, plasma bacteria killing capacity). Intriguingly, individuals with more repeatable IFN-γ and lymphocyte levels were at a significantly higher risk of acquiring TB infection. In stark contrast, average IFN-γ and lymphocyte levels were poor predictors of TB risk, indicating that immune variability rather than absolute response level better captured variation in disease susceptibility. This work highlights the important and under-appreciated role of immune variability as a predictor of infection risk.

Parasite sharing in wild ungulates and their predators: Effects of phylogeny, range overlap, and trophic links.

Understanding factors that facilitate interspecific pathogen transmission is a central issue for conservation, agriculture, and human health. Past work showed that host phylogenetic relatedness and geographical proximity can increase cross-species transmission, but further work is needed to examine the importance of host traits, and species interactions such as predation, in determining the degree to which parasites are shared between hosts. Here we consider the factors that predict patterns of parasite sharing across a diverse assemblage of 116 wild ungulates (i.e., hoofed mammals in the Artiodactyla and Perissodactyla) and nearly 900 species of micro- and macroparasites, controlling for differences in total parasite richness and host sampling effort. We also consider the effects of trophic links on parasite sharing between ungulates and carnivores. We tested for the relative influence of range overlap, phylogenetic distance, body mass, and ecological dissimilarity (i.e., the distance separating species in a Euclidean distance matrix based on standardized traits) on parasite sharing. We also tested for the effects of variation in study effort as a potential source of bias in our data, and tested whether carnivores reported to feed on ungulates have more ungulate parasites than those that use other resources. As in other groups, geographical range overlap and phylogenetic similarity predicted greater parasite community similarity in ungulates. Ecological dissimilarity showed a weak negative relationship with parasite sharing. Counter to our expectations, differences, not similarity, in host body mass predicted greater parasite sharing between pairs of ungulate hosts. Pairs of well-studied host species showed higher overlap than poorly studied species, although including sampling effort did not reduce the importance of biological traits in our models. Finally, carnivores that feed on ungulates harboured a greater richness of ungulate helminths. Overall, we show that the factors that predict parasite sharing in wild ungulates are similar to those known for other mammal groups, and demonstrate the importance of controlling for heterogeneity in host sampling effort in future analyses of parasite sharing. We also show that ecological interactions, in this case trophic links via predation, can allow sharing of some parasite species among distantly related host species.

Social living simultaneously increases infection risk and decreases the cost of infection.

Elevated parasite infection risk is considered to be a near-universal cost of social living. However, living in groups may also provide benefits that reduce the negative impacts of infection. These potential 'tolerance' benefits of living socially are theoretically possible, but have rarely been described. In this study, we used an anthelmintic treatment experiment in wild Grant's gazelles (Nanger granti), who are commonly infected with gastrointestinal nematodes (GIN), to show that social living confers both costs and benefits related to GIN parasitism. We show that although larger group size increases GIN infection risk, a key cost of GIN infection-the suppression of food intake-is simultaneously moderated by living in larger groups. Our findings help illuminate the complex role parasites play in the evolution of host social behaviour.

Global Mammal Parasite Database version 2.0.

Illuminating the ecological and evolutionary dynamics of parasites is one of the most pressing issues facing modern science, and is critical for basic science, the global economy, and human health. Extremely important to this effort are data on the disease-causing organisms of wild animal hosts (including viruses, bacteria, protozoa, helminths, arthropods, and fungi). Here we present an updated version of the Global Mammal Parasite Database, a database of the parasites of wild ungulates (artiodactyls and perissodactyls), carnivores, and primates, and make it available for download as complete flat files. The updated database has more than 24,000 entries in the main data file alone, representing data from over 2700 literature sources. We include data on sampling method and sample sizes when reported, as well as both "reported" and "corrected" (i.e., standardized) binomials for each host and parasite species. Also included are current higher taxonomies and data on transmission modes used by the majority of species of parasites in the database. In the associated metadata we describe the methods used to identify sources and extract data from the primary literature, how entries were checked for errors, methods used to georeference entries, and how host and parasite taxonomies were standardized across the database. We also provide definitions of the data fields in each of the four files that users can download.

A comparison of two methods for quantifying parasitic nematode fecundity.

Accurate measures of nematode fecundity can provide important information for investigating parasite life history evolution, transmission potential, and effects on host health. Understanding differences among fecundity assessment protocols and standardizing methods, where possible, will enable comparisons across different studies and host and parasite species and systems. Using the trichostrongyle nematode Cooperia fuelleborni isolated from wild African buffalo (Syncerus caffer), we compared egg recovery and enumeration between two methods for measuring the fecundity of female worms. The first method, in utero egg count, involves visual enumeration of the eggs via microscopic inspection of the uterine system. The second method, ex utero egg count, involves dissolving the same specimens from above in a sodium chloride solution to release the eggs from the female's uterus, then enumeration under an inverted microscope. On average, the ex utero method resulted in 34% more eggs than the in utero method. However, results indicate that the two methods used to quantify parasitic nematode fecundity are highly correlated. Thus, while both methods are viable options for estimating relative nematode fecundity, we recommend caution in undertaking comparative studies that utilize egg count data collected using different methods.

The macroecology of infectious diseases: a new perspective on global-scale drivers of pathogen distributions and impacts.

Identifying drivers of infectious disease patterns and impacts at the broadest scales of organisation is one of the most crucial challenges for modern science, yet answers to many fundamental questions remain elusive. These include what factors commonly facilitate transmission of pathogens to novel host species, what drives variation in immune investment among host species, and more generally what drives global patterns of parasite diversity and distribution? Here we consider how the perspectives and tools of macroecology, a field that investigates patterns and processes at broad spatial, temporal and taxonomic scales, are expanding scientific understanding of global infectious disease ecology. In particular, emerging approaches are providing new insights about scaling properties across all living taxa, and new strategies for mapping pathogen biodiversity and infection risk. Ultimately, macroecology is establishing a framework to more accurately predict global patterns of infectious disease distribution and emergence.

Reciprocal relationships between behaviour and parasites suggest that negative feedback may drive flexibility in male reproductive behaviour.

Parasites are ubiquitous components of the environment that contribute to behavioural and life-history variation among hosts. Although it is well known that host behaviour can affect parasite infection risk and that parasites can alter host behaviour, the potential for dynamic feedback between these processes is poorly characterized. Using Grant's gazelle (Nanger granti) as a model, we tested for reciprocal effects of behaviour on parasites and parasites on behaviour to understand whether behaviour-parasite feedback could play a role in maintaining variation in male reproductive behaviour. Adult male gazelles either defend territories to attract mates or reside in bachelor groups. Territoriality is highly variable both within- and between-individuals, suggesting that territory maintenance is costly. Using a combination of longitudinal and experimental studies, we found that individual males transition frequently between territorial and bachelor reproductive status, and that elevated parasite burdens are a cost of territoriality. Moreover, among territorial males, parasites suppress aspects of behaviour related to territory maintenance and defence. These results suggest that territorial behaviour promotes the accumulation of parasites in males, and these parasites dampen the very behaviours required for territory maintenance. Our findings suggest that reciprocal feedback between host behaviour and parasitism could be a mechanism maintaining variation in male reproductive behaviour in the system.

Host behaviour-parasite feedback: an essential link between animal behaviour and disease ecology.

Animal behaviour and the ecology and evolution of parasites are inextricably linked. For this reason, animal behaviourists and disease ecologists have been interested in the intersection of their respective fields for decades. Despite this interest, most research at the behaviour-disease interface focuses either on how host behaviour affects parasites or how parasites affect behaviour, with little overlap between the two. Yet, the majority of interactions between hosts and parasites are probably reciprocal, such that host behaviour feeds back on parasites and vice versa. Explicitly considering these feedbacks is essential for understanding the complex connections between animal behaviour and parasite ecology and evolution. To illustrate this point, we discuss how host behaviour-parasite feedbacks might operate and explore the consequences of feedback for studies of animal behaviour and parasites. For example, ignoring the feedback of host social structure on parasite dynamics can limit the accuracy of predictions about parasite spread. Likewise, considering feedback in studies of parasites and animal personalities may provide unique insight about the maintenance of variation in personality types. Finally, applying the feedback concept to links between host behaviour and beneficial, rather than pathogenic, microbes may shed new light on transitions between mutualism and parasitism. More generally, accounting for host behaviour-parasite feedbacks can help identify critical gaps in our understanding of how key host behaviours and parasite traits evolve and are maintained.

Experimental insight into the process of parasite community assembly.

Community assembly is a fundamental process that has long been a central focus in ecology. Extending community assembly theory to communities of co-infecting parasites, we used a gastrointestinal nematode removal experiment in free-ranging African buffalo to examine the community assembly patterns and processes. We first asked whether reassembled communities differ from undisturbed communities by comparing anthelmintic-treated and control hosts. Next, we examined the temporal dynamics of assembly using a cross-section of communities that reassembled for different periods of time since last experimental removal. Next, we tested for evidence of assembly processes that might drive such reassembly patterns: environmental filtering based on host traits (i.e. habitat patches), interspecific interactions, priority effects and chance dispersal from the environmental pool of infective stages (i.e. the regional species pool). On average, reassembled parasite communities had lower abundance, but were more diverse and even, and these patterns varied tightly with reassembly time. Over time, the communities within treated hosts progressively resembled controls as diversity and evenness decreased, while total abundance increased. Notably, experimental removal allowed us to attribute observed differences in abundance, diversity and evenness to the process of community assembly. During early reassembly, parasite accumulation was biased towards a subordinate species and, by excluding stochastic assembly processes (i.e. chance dispersal and priority effects), we were able to determine that early assembly is deterministic. Later in the reassembly process, we established that host traits, as well as stochastic dispersal from the environmental pool of infective stages, can affect the community composition. Overall, our results suggest that there is a high degree of resiliency and environmental dependence to the worm communities of buffalo. More generally, our data show that both deterministic and stochastic processes may play a role in the assembly of parasite communities of wild hosts, but their relative importance may vary temporally. Consequently, the best strategy for managing reassembling parasite communities may also need to shift over time.